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The Werribee Football Club was established in 1964 as part of a bid to enter the Victorian Football Association in 1965. The new club was formed as an amalgamation of four local clubs which competed in the Werribee District Football League: Werribee South, Irish National Foresters, Services and Metro Farm.[2] In the early years the team was in the second division, and had little success over that time. Geographically distant from all other clubs in what was then a small town partway between Melbourne and Geelong, the club was unable to attract many strong non-local players, and was considered "the lonesome battler" of the Association. Up to 1980, the club had struggled through its sixteen seasons in Division 2 for one finals appearance and four wooden spoons.[3] Its sole success during this time was its victory in the 1978 lightning premiership; it was the only Division 2 club to win that competition during its eight-year existence.[4]

The club embarked on a five-year plan in the late 1970s, which saw the club build its finances, improve its on-field performance to reach the finals in 1981, and open a $200k social club in 1980.[3] This saw the club promoted to Division 1 in 1982, as part of the Association's merit-based restructure of the competition. The club was relegated after finishing last at the end of 1985.[5] The club won the Division 2 minor premiership in 1987,[6] but never won a premiership or even a finals match during its time in Division 2.[7]

In December 1986, Werribee had been earmarked for exclusion under the Association's controversial Football Organisation Review Team (FORT) recommendations, which sought to rationalise the Association to a stronger twelve-club competition in a single division, but which were never formally enacted after being rejected by the clubs.[8] However, after the VFA had contracted to a single division in 1989, Werribee began to enjoy on-field success, and Werribee was one of only two of the FORT review's excluded clubs to survive in the VFA beyond 1991, the other being Springvale.

The club played a major role in the finals during the early 1990s, winning the premiership in 1993, finishing as runner-up after winning the minor premiership in 1991, and playing in a total of five finals series from 1990 to 1995.

At the end of the 1995 season, the club faced another threat to its survival when the Victorian State Football League sought to align the VFA (which at that time renamed the VFL) with the TAC Cup, and needed only one western suburban team to align with the Western Jets. Werribee and Williamstown were ordered to merge;[9] when they could not agree to terms, the VSFL decided to grant the remaining licence to Williamstown, resulting in Werribee's expulsion from the VFL.[10] After Werribee supporters rallied and the club demonstrated a strong position to launch legal action, the VSFL reinstated Werribee's licence under then-unique conditions which left it as the only club without district and TAC Cup feeder teams.[11] The conditions did not harm the club on-field, as it continued to perform strongly, reaching the finals for the next four years, including winning the minor premiership and making a losing Grand Final appearance in 1998. The club was later permitted to take on the Geelong Falcons as its TAC Cup feeder team.[12]

Following the amalgamation of the AFL reserves and the VFL, Werribee entered a reserves affiliation with the AFL's Western Bulldogs, which lasted from 2000 to 2007. The alliance allowed the club to have access to Bulldogs players who were not selected in the senior team. During that time, the club reached a further two Grand Finals in the 2000s: in 2001 and 2005, but lost both. From 2008 until 2015, the club was part of a split-affiliation structure with the North Melbourne Football Club, whereby half of North Melbourne's reserve players were allocated to Werribee and half were allocated to North Ballarat. From 2016 and 2017, the club was fully affiliated with North Melbourne and have access to all North Melbourne reserves players.[13]

In 2018 the club is again a standalone club like Port Melbourne, Williamstown and Coburg.[14]